Gerald D. schmidt & Larry S. Roberts’ Foundations of parasitology Fascioloides magna, a very large liver fluke that parasitizes deer and cattle (p. 272). The body of this specimen was rendered transpar- ent, leaving only pigment in its intestinal tract visible. An enlarger was used to project an image directly onto photographic paper, which after development clearly shows the trematode’s highly branched gut. Courtesy of William C. Campbell eighth edition

Gerald D. schmidt & Larry S. Roberts’ Foundations of parasitology

larry s. roberts florida international university john janovy, jr. University of nebraska–lincoln GERALD D. SCHMIDT & LARRY S. ROBERTS’ FOUNDATIONS OF PARASITOLOGY EIGHTH EDITION

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ISBN 978–0–07–302827–9 MHID 0–07–302827–4

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Library of Congress Cataloging-in-Publication Data

Roberts, Larry S., 1935- Gerald D. Schmidt & Larry S. Roberts’ foundations of parasitology / Larry S. Roberts, John Janovy, Jr. — 8th ed. p. cm. Includes index. ISBN 978-0-07-302827-9 — ISBN 0-07-302827-4 (hard copy : alk. paper) 1. Parasitology. I. Janovy, John, 1937- II. Title. III. Title: Gerald D. Schmidt and Larry S. Roberts’ foundations of parasitology. IV. Title: Foundations of parasitology. QL757.R585 2009 591.7'857—dc22 2008031997

www.mhhe.com about the authors

ative accomplishments consist of approximately 90 scientific LARRY S. ROBERTS papers and book chapters; 14 books, including Keith County Journal, On Becoming a Biologist, Teaching in Eden, Out- Larry S. Roberts, professor witting College Professors, and Foundations of Parasitology emeritus of biology at Texas (with Larry Roberts); the screenplay for the televised version Tech University and an adjunct of Keith County Journal (Nebraska Public Television); and professor at Florida Interna- numerous popular articles. His teaching experiences include tional University, has exten- almost continuous service in the large-enrollment freshman sive experience teaching biology course; Field Parasitology (BIOS 487/887) at the parasitology, invertebrate zool- Cedar Point Biological Station; Invertebrate Zoology (BIOS ogy, marine biology, and de- 381); Parasitology (BIOS 385); a decade in BIOS 103/204 velopmental biology. He (Organismic Biology/Biodiversity); and numerous honors received his ScD in parasitol- seminars. He has supervised 18 MS students, 14 PhD stu- ogy at Johns Hopkins Univer- dents, and approximately 50 undergraduate researchers, in- sity and has co-authored cluding 10 Howard Hughes scholars. His honors include the Foundations of Parasitology University of Nebraska Distinguished Teaching Award from the first edition through (1970), University Honors Program Master Lecturer (1986), this, the eighth edition. He is American Health magazine book award (1987, for Fields of also co-author of Integrated Principles of Zoology, Biology of Friendly Strife), University of Nebraska Outstanding Re- Animals, and Animal Diversity, and is author of The Underwa- search and Creativity Award (1998), The Nature Conser- ter World of Sport Diving. vancy Hero recognition (2000), and the American Society of Dr. Roberts has published many research articles and re- Parasitologists Clark P. Read Mentorship Award (2003). views. He has served as president of the American Society of Parasitologists, Southwestern Association of Parasitologists, and Southeastern Society of Parasitologists, and is a member of GERALD D. SCHMIDT numerous other professional societies. He received the Henry Baldwin Ward Medal from the American Society of Parasitolo- Gerald D. Schmidt was pro- gists. Dr. Roberts also serves on the editorial board of the jour- fessor of biology at the Uni- Parasitology Research nal . His hobbies include scuba diving, versity of Northern Colorado underwater photography, and tropical horticulture. (UNC) when he passed away. Dr. Roberts can be contacted at: Lroberts1@compuserve He received his PhD from .com Colorado State University. He was active in research and promoting research activities JOHN JANOVY, JR. at UNC, and he published more than 160 research arti- John Janovy, Jr. (PhD Uni- cles in scientific journals, as versity of Oklahoma, 1965) is well as six books. He re- the Paula and D. B. Varner ceived awards from UNC for Distinguished Professor of outstanding teaching and for Biological Sciences at the distinguished scholarship. He University of Nebraska–Lin- was a board member of the World Federation of Parasitolo- coln. His research interest is gists; a Fellow of the Royal Society of Tropical Medicine parasitology, with particular and Hygiene, London; and a Fellow of the Royal Society of focus on parasite ecology and South Australia. life cycles. He has been direc- Dr. Schmidt served the American Society of Parasitolo- tor of the Cedar Point Biolog- gists as secretary-treasurer for seven years. He was co-author ical Station, interim director of Foundations of Parasitology through the first four edi- of the University of Nebraska tions. His hobbies were hunting and fishing, especially fish- State Museum, and an assis- ing, and he wrote a book on fishing. tant dean of Arts and Sci- Dr. Schmidt died on 16 October 1990; many more de- ences, and he is currently the secretary-treasurer of the tails of his life can be found in the Journal of Parasitology, American Society of Parasitologists. His scholarly and cre- 78:757–773.

v brief contents

23 Nematodes: Trichinellida and Dioctophymatida, Preface xv Enoplean Parasites 399 24 Nematodes: Tylenchina, Pioneering 1 Introduction to Parasitology 1 Parasites 413 2 Basic Principles and Concepts I: Parasite 25 Nematodes: Strongyloidea, Bursate Systematics, Ecology,and Evolution 11 Rhabditidans 419 3 Basic Principles and Concepts II: Immunology 26 Nematodes: Ascaridomorpha, Intestinal Large and Pathology 25 Roundworms 433 4 Parasitic Protozoa: Form, Function, 27 Nematodes: Oxyuridomorpha, and Classification 43 Pinworms 447 5 Kinetoplasta: Trypanosomes and Their 28 Nematodes: Gnathostomatomorpha and Kin 61 Spiruromorpha, a Potpourri 453 6 Other Flagellated Protozoa 89 29 Nematodes: Filaroidea, Filarial Worms 463 7 The Amebas 107 30 Nematodes: Dracunculoidea, Guinea Worms, 8 Phylum Apicomplexa: Gregarines, Coccidia, and Others 479 and Related Organisms 123 31 Phylum Nematomorpha, Hairworms 487 9 Phylum Apicomplexa: Malaria Organisms 32 Phylum Acanthocephala: Thorny-Headed and Piroplasms 147 Worms 495 10 Phylum Ciliophora: Ciliated Protistan 33 Phylum Arthropoda: Form, Function, Parasites 175 and Classification 513 11 Microsporidia and Myxozoa: Parasites with Polar 34 Parasitic Crustaceans 537 Filaments 183 35 Pentastomida: Tongue Worms 561 12 The Mesozoa: Pioneers or Degenerates? 195 36 Parasitic Insects: Phthiraptera, Chewing 13 Introduction to Phylum and Sucking Lice 569 Platyhelminthes 201 37 Parasitic Insects: Hemiptera, Bugs 581 14 Trematoda: Aspidobothrea 211 38 Parasitic Insects: Fleas, Order 15 Trematoda: Form, Function, and Classification Siphonaptera 589 of Digeneans 219 39 Parasitic Insects: Diptera, Flies 601 16 Digeneans: Strigeiformes 247 40 Parasitic Insects: Strepsiptera, Hymenoptera, 17 Digeneans: Echinostomatiformes 265 and Others 627 18 Digeneans: Plagiorchiformes and 41 Parasitic Arachnids: Subclass Acari, Ticks Opisthorchiformes 277 and Mites 639 19 Monogenoidea 295 20 Cestoidea: Form, Function, and Classification of Tapeworms 313 Glossary 661 21 Tapeworms 341 Index 683 22 Phylum Nematoda: Form, Function, and Classification 369 contents

Preface xv Basis of Self and Nonself Recognition in Adaptive Responses 30 Antibodies 30 Lymphocytes 31 1 Introduction to Parasitology 1 Subsets of T Cells 31 T-Cell Receptors 32 Relationship of Parasitology to Other Generation of a Humoral Response 32 Sciences 1 Cell-mediated Response 33 Some Basic Definitions 2 Inflammation 34 Interactions of Symbionts 2 Acquired Immune Deficiency Syndrome Hosts 4 (AIDS) 35 Parasitology and Human Welfare 4 Immunodiagnosis 35 Parasites of Domestic and Wild Animals 6 Pathogenesis of Parasitic Infections 36 Parasitology for Fun and Profit 7 Accommodation and Tolerance in the Host- Careers in Parasitology 7 Parasite Relationship 38 References 8 Overview 39 Additional References 9 References 41 Parasitology on the World Wide Web 9 Additional References 42

2 Basic Principles and Concepts I: Parasite Systematics, Ecology,and Evolution 11 4 Parasitic Protozoa: Form, Function, and Classification 43 Systematics and Taxonomy of Parasites 11 Parasite Ecology 12 Form and Function 43 The Host as an Environment 12 Nucleus and Cytoplasm 44 A Parasite’s Ecological Niche 12 Locomotor Organelles 46 Parasite Populations 14 Reproduction and Life Cycles 50 Trophic Relationships 16 Encystment 51 Adaptations for Transmission 16 Feeding and Metabolism 52 Epidemiology 19 Excretion and Osmoregulation 53 Mathematical Models 20 Endosymbionts 53 Parasite Evolution 20 Classification of Protozoan Phyla 54 Evolutionary Associations Between Parasites and Characters Generally Shared by Amebas 56 Hosts 20 Stramenopiles 57 Parasitism and Sexual Selection 22 References 60 Evolution of Virulence 22 Additional References 60 References 23 Additional References 24

5 Kinetoplasta: Trypanosomes 3 and Their Kin 61 Basic Principles and Concepts II: Forms of Trypanosomatidae 61 Immunology and Pathology 25 Genus Trypanosoma 64 Susceptibility and Resistance 25 Section Salivaria 65 Innate Defense Mechanisms 26 Section Stercoraria 70 Cell Signaling 26 Genus Leishmania 77 Cellular Defenses: Phagocytosis 29 Cutaneous Leishmaniasis 79 Adaptive Immune Response Visceral Leishmaniasis 82 of Vertebrates 30 Other Trypanosomatid Parasites 85

vii viii Contents

Genus Leptomonas 85 Genus Herpetomonas 85 9 Phylum Apicomplexa: Malaria Organisms Genus Crithidia 85 and Piroplasms 147 Genus Blastocrithidia 85 Genus Phytomonas 85 Order Haemospororida 147 References 85 Genus Plasmodium 147 Additional References 88 Genus Haemoproteus 164 Genus Leucocytozoon 165 Order Piroplasmida 166 Family Babesiidae 166 Family Theileriidae 169 6 Other Flagellated Protozoa 89 References 170 Order Retortamonadida 89 Additional References 173 Family Retortamonadidae 89 Order Diplomonadida 90 Family Hexamitidae 90 Trichomonads (Class Trichomonada, Order 10 Phylum Ciliophora: Ciliated Protistan Trichomonadida) 95 Parasites 175 Family Trichomonadidae 95 Family Monocercomonadidae 100 Class Spirotrichea 175 Order Opalinida (Slopalinida) 103 Order Clevelandellida, Family Nyctotheridae 175 Family Opalinidae 103 Class Litostomatea 176 References 104 Order Vestibuliferida, Family Balantidiidae 176 Additional References 106 Order Entodiniomorphida 177 Class Oligohymenophorea 178 Subclass Hymenostomatia, Order Hymenostomatida, Family Ichthyophthiriidae 178 7 The Amebas 107 Subclass Peritrichia 178 Order Sessilida 178 Amebas Infecting Mouth Order Mobilida, Family Trichodinidae 178 and Intestine 107 References 180 Family Entamoebidae 107 Additional References 181 Amebas Infecting Brain and Eyes 116 Family Vahlkampfiidae 116 Family Acanthamoebidae 118 Amebas of Uncertain Affinities 119 References 120 11 Microsporidia and Myxozoa: Parasites Additional References 122 with Polar Filaments 183

Phylum Microsporidia 183 Family Nosematidae 185 Other Microsporidian Species 185 8 Phylum Apicomplexa: Gregarines, Coccidia, Epidemiology and Zoonotic Potential 186 and Related Organisms 123 Myxozoa 186 Family Myxobolidae 187 Apicomplexan Structure 123 References 192 Class Conoidasida, Subclass Additional References 193 Gregarinasina 124 Order Eugregarinorida 125 Subclass Coccidiasina 126 Order Eucoccidiorida 127 Suborder Adeleorina 127 12 The Mesozoa: Pioneers or Suborder Eimeriorina 128 Degenerates? 195 References 144 Additional References 146 Phylum Dicyemida 195 Class Rhombozoa 195 Contents ix

Phylum Orthonectida 197 Development 229 Class Orthonectida 197 Embryogenesis 230 Phylogenetic Position 199 Larval and Juvenile Development 230 Host-Parasite Relationships 199 Development in a Definitive Host 235 References 200 Trematode Transitions 236 Additional References 200 Summary of Life Cycle 237 Metabolism 237 Energy Metabolism 237 Synthetic Metabolism 240 13 Introduction to Phylum Biochemistry of Trematode Tegument 240 Platyhelminthes 201 Phylogeny of Digenetic Trematodes 240 References 243 Platyhelminth Systematics 202 Additional References 245 Turbellarians 206 Acoels 206 Rhabditophorans 206 Temnocephalideans 207 Alloeocoels 208 16 Digeneans: Strigeiformes 247 Tricladids 208 Polycladids 208 Superfamily Strigeoidea 247 References 208 Family Diplostomidae 247 Additional References 210 Family Strigeidae 248 Superfamily Schistosomatoidea 249 Family Schistosomatidae: Schistosoma Species and Schistosomiasis 250 14 Trematoda: Aspidobothrea 211 Control 260 References 263 Form and Function 211 Additional References 264 Body Form 211 Tegument 211 Digestive System 212 Osmoregulatory System 212 Nervous System 212 17 Digeneans: Echinostomatiformes 265 Reproductive Systems 213 Superfamily Echinostomatoidea 265 Development 214 Family Echinostomatidae 265 Aspidogaster conchicola 216 Echinostomatids as Models in Experimental Rugogaster hydrolagi 217 Parasitology 267 Stichocotyle nephropsis 217 Family Fasciolidae 268 Phylogenetic Considerations 217 Other Fasciolid Trematodes 271 References 218 Family Cathaemasiidae 273 Additional References 218 Superfamily Paramphistomoidea 274 Family Paramphistomidae 274 Family Diplodiscidae 274 15 Family Gastrodiscidae 275 Trematoda: Form, Function, References 275 and Classification of Digeneans 219 Additional References 276 Form and Function 219 Body Form 219 Tegument 220 Muscular System 223 18 Digeneans: Plagiorchiformes Nervous System 224 and Opisthorchiformes 277 Excretion and Osmoregulation 225 Acquisition of Nutrients and Digestion 227 Order Plagiorchiformes 277 Reproductive Systems 228 Suborder Plagiorchiata 277